Cell type specific transcriptional reprogramming of maize leaves during Ustilago maydis induced tumor formation

Abstract

Ustilago maydis is a biotrophic pathogen and well-established genetic model to understand the molecular basis of biotrophic interactions. U. maydis suppresses plant defense and induces tumors on all aerial parts of its host plant maize. In a previous study we found that U. maydis induced leaf tumor formation builds on two major processes: the induction of hypertrophy in the mesophyll and the induction of cell division (hyperplasia) in the bundle sheath. In this study we analyzed the cell-type specific transcriptome of maize leaves 4 days post infection. This analysis allowed identification of key features underlying the hypertrophic and hyperplasic cell identities derived from mesophyll and bundle sheath cells, respectively. We examined the differentially expressed (DE) genes with particular focus on maize cell cycle genes and found that three A-type cyclins, one B-, D- and T-type are upregulated in the hyperplasic tumorous cells, in which the U. maydis effector protein See1 promotes cell division. Additionally, most of the proteins involved in the formation of the pre-replication complex (pre-RC, that assure that each daughter cell receives identic DNA copies), the transcription factors E2F and DPa as well as several D-type cyclins are deregulated in the hypertrophic cells.

Roles of plant retinoblastoma protein: cell cycle and beyond

“…Irrespective of the whether infections impinge only on the RBR1 pathway or also other pathways, profound changes in the host cells are a primary outcome (Hanley‐Bowdoin et al , ; Ascencio‐Ibanez et al , ). Modulation of the RBR1 pathway is also seen with various other types of pathogens (Depuydt et al , ; Stes et al , ; Wen et al , ; Villajuana‐Bonequi et al , ). An unexpected link between the effector‐triggering immunity (ETI), and its associated programmed cell death, and the RBR1‐ERF module has been reported.…”

Transcriptome analysis in the maize-Ustilago maydis interaction identifies maize-line-specific activity of fungal effectors

“…The reactivation of cell division processes including DNA replication are crucial for formation of U. maydis-induced tumours (Doehlemann et al 2008b; Redkar et al 2015; Matei et al 2018; Villajuana-Bonequi et al 2019). Hence, enrichment of such processes in more susceptible maize lines is not surprising since there, U. maydis induces more and larger tumours compared to the more resistant lines.…”

“…Correlation analysis of gene expression to resistance levels via WGCNA again identified processes involved in protein phosphorylation, as well as cell division being upregulated in the more susceptible maize lines in response to U. maydis . To build a tumour, the fungus actively triggers cell division and reactivates DNA synthesis in the leaf tissue, which goes along with alterations of genes involved in cell-cycle regulation (Redkar et al 2015; Matei et al 2018; Villajuana-Bonequi et al 2019). In the A. thaliana-Plasmodiophora brassicae interaction, which is also accompanied by gall formation, genes involved in cell proliferation were found to be associated with QDR (Jubault et al 2013).…”

Beyond What Your Retina Can See: Similarities of Retinoblastoma Function between Plants and Animals, from Developmental Processes to Epigenetic Regulation

“…In addition, ZmRBR3/4 transcripts accumulate in mitotic tissues from the endosperm. Recently, high levels of ZmRBR3/4 were found in tumor-like formations (induced by the fungus Ustilago maydis) from maize leaves [118,123]. Interestingly, the protein complex ZmRBR3/4/E2F has a unique role not observed in other plants or animals: high levels of ZmRBR3/4 in complex with E2F promotes the expression of genes involved in DNA replication and cell cycle At about the same time that the pRb ortholog in plants was discovered, homologs of other components of the animal's cell cycle regulatory machinery were identified and characterized in corn, as well as in Arabidopsis and Medicago sativa (alfalfa) [61,[108][109][110][111].…”